Activation of the Type I Interferon Pathway Is Enhanced in Response to Human Neuronal Differentiation

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Farmer, Jocelyn R ^a   Altschaefl, Kate M ^a   O'Shea, K Sue ^a   Miller, David J ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERFERON; INTERFERON RECEPTOR; INTERFERON RECEPTOR SUBUNIT 2; INTERFERON REGULATORY FACTOR 9; MESSENGER RNA; STAT1 PROTEIN; STAT2 PROTEIN; UNCLASSIFIED DRUG;

ALPHAVIRUS INFECTION; ANTIVIRAL ACTIVITY; ARTICLE; CELL MATURATION; CELL PROTECTION; CELL VIABILITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; EMBRYO; HUMAN; HUMAN CELL; IMMUNE RESPONSE; INNATE IMMUNITY; MOLECULAR DYNAMICS; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NONHUMAN; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UPREGULATION; VIRUS CELL INTERACTION; WESTERN EQUINE ENCEPHALOMYELITIS ALPHAVIRUS;

CELL DIFFERENTIATION; CELL LINE; EMBRYONIC STEM CELLS; GENE EXPRESSION; GENE ORDER; HUMANS; IMMUNITY, INNATE; INTERFERON TYPE I; NEURAL STEM CELLS; NEURONS; RECEPTOR, INTERFERON ALPHA-BETA; RNA, MESSENGER; SIGNAL TRANSDUCTION; STAT2 TRANSCRIPTION FACTOR;

EID: 84874671108     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0058813     Document Type: Article

References (73)

1. Peltier DC, Simms A, Farmer JR, Miller DJ, (2010) Human neuronal cells possess functional cytoplasmic and TLR-mediated innate immune pathways influenced by phosphatidylinositol-3 kinase signaling. J Immunol 184: 7010-7021.
2. Daffis S, Samuel MA, Suthar MS, Gale M Jr, Diamond MS, (2008) Toll-like receptor 3 has a protective role against West Nile virus infection. J Virol 82: 10349-10358.
3. Menager P, Roux P, Megret F, Bourgeois JP, Le Sourd AM, et al. (2009) Toll-like receptor 3 (TLR3) plays a major role in the formation of rabies virus Negri Bodies. PLoS Pathog 5: e1000315.
4. Zhou Y, Ye L, Wan Q, Zhou L, Wang X, et al. (2009) Activation of Toll-like receptors inhibits herpes simplex virus-1 infection of human neuronal cells. J Neurosci Res 87: 2916-2925.
5. Delhaye S, Paul S, Blakqori G, Minet M, Weber F, et al. (2006) Neurons produce type I interferon during viral encephalitis. Proc Natl Acad Sci U S A 103: 7835-7840.
6. Castorena KM, Peltier DC, Peng W, Miller DJ, (2008) Maturation-dependent responses of human neuronal cells to western equine encephalitis virus infection and type I interferons. Virology 372: 208-220.
7. Samuel MA, Diamond MS, (2005) α/β interferon protects against lethal West Nile virus infection by restricting cellular tropism and enhancing neuronal survival. J Virol 79: 13350-13361.
8. Burdeinick-Kerr R, Griffin DE, (2005) γ interferon-dependent, noncytolytic clearance of Sindbis virus infection from neurons in vitro. J Virol 79: 5374-5385.
9. Ryman KD, Klimstra WB, Nguyen KB, Biron CA, Johnston RE, (2000) α/β interferon protects adult mice from fatal Sindbis virus infection and is an important determinant of cell and tissue tropism. J Virol 74: 3366-3378.
10. White LJ, Wang JG, Davis NL, Johnston RE, (2001) Role of α/β interferon in Venezuelan equine encephalitis virus pathogenesis: effect of an attenuating mutation in the 5′ untranslated region. J Virol 75: 3706-3718.
11. Detje CN, Meyer T, Schmidt H, Kreuz D, Rose JK, et al. (2009) Local type I IFN receptor signaling protects against virus spread within the central nervous system. J Immunol 182: 2297-2304.
12. Gubler DJ, (2002) The global emergence/resurgence of arboviral diseases as public health problems. Arch Med Res 33: 330-342.
13. Weaver SC, Reisen WK, (2010) Present and future arboviral threats. Antiviral Res 85: 328-345.
14. Lowry PW, (1997) Arbovirus encephalitis in the United States and Asia. J Lab Clin Med 129: 405-411.
15. Vernon PS, Griffin DE, (2005) Characterization of an in vitro model of alphavirus infection of immature and mature neurons. J Virol 79: 3438-3447.
16. Pekosz A, Phillips J, Pleasure D, Merry D, Gonzalez-Scarano F, (1996) Induction of apoptosis by La Crosse virus infection and role of neuronal differentiation and human bcl-2 expression in its prevention. J Virol 70: 5329-5335.
17. Tsueng G, Tabor-Godwin JM, Gopal A, Ruller CM, Deline S, et al. (2011) Coxsackievirus preferentially replicates and induces cytopathic effects in undifferentiated neural progenitor cells. J Virol 85: 5718-5732.
18. Luo MH, Schwartz PH, Fortunato EA, (2008) Neonatal neural progenitor cells and their neuronal and glial cell derivatives are fully permissive for human cytomegalovirus infection. J Virol 82: 9994-10007.
19. Kosugi I, Shinmura Y, Kawasaki H, Arai Y, Li RY, et al. (2000) Cytomegalovirus infection of the central nervous system stem cells from mouse embryo: a model for developmental brain disorders induced by cytomegalovirus. Lab Invest 80: 1373-1383.
20. Lawrence DM, Durham LC, Schwartz L, Seth P, Maric D, et al. (2004) Human immunodeficiency virus type 1 infection of human brain-derived progenitor cells. J Virol 78: 7319-7328.
21. Krathwohl MD, Kaiser JL, (2004) HIV-1 promotes quiescence in human neural progenitor cells. J Infect Dis 190: 216-226.
22. Feuer R, Pagarigan RR, Harkins S, Liu F, Hunziker IP, et al. (2005) Coxsackievirus targets proliferating neuronal progenitor cells in the neonatal CNS. J Neurosci 25: 2434-2444.
23. Das S, Basu A, (2008) Japanese encephalitis virus infects neural progenitor cells and decreases their proliferation. J Neurochem 106: 1624-1636.
24. Brnic D, Stevanovic V, Cochet M, Agier C, Richardson J, et al. (2012) Borna disease virus infects human neural progenitor cells and impairs neurogenesis. J Virol 86: 2512-2522.
25. Odeberg J, Wolmer N, Falci S, Westgren M, Seiger A, et al. (2006) Human cytomegalovirus inhibits neuronal differentiation and induces apoptosis in human neural precursor cells. J Virol 80: 8929-8939.
26. Luo MH, Hannemann H, Kulkarni AS, Schwartz PH, O'Dowd JM, et al. (2010) Human cytomegalovirus infection causes premature and abnormal differentiation of human neural progenitor cells. J Virol 84: 3528-3541.
27. Rehberg E, Kelder B, Hoal EG, Pestka S, (1982) Specific molecular activities of recombinant and hybrid leukocyte interferons. J Biol Chem 257: 11497-11502.
28. Zhang SC, Wernig M, Duncan ID, Brustle O, Thomson JA, (2001) In vitro differentiation of transplantable neural precursors from human embryonic stem cells. Nat Biotechnol 19: 1129-1133.
29. Itsykson P, Ilouz N, Turetsky T, Goldstein RS, Pera MF, et al. (2005) Derivation of neural precursors from human embryonic stem cells in the presence of noggin. Mol Cell Neurosci 30: 24-36.
30. Peng W, Peltier DC, Larsen MJ, Kirchhoff PD, Larsen SD, et al. (2009) Identification of thieno [3,2-b] pyrrole derivatives as novel small molecule inhibitors of neurotropic alphaviruses. J Infect Dis 199: 950-957.
31. Weiss JN, (1997) The Hill equation revisited: uses and misuses. FASEB J 11: 835-841.
32. Huh GS, Boulanger LM, Du H, Riquelme PA, Brotz TM, et al. (2000) Functional requirement for class I MHC in CNS development and plasticity. Science 290: 2155-2159.
33. Neumann H, Cavalie A, Jenne DE, Wekerle H, (1995) Induction of MHC class I genes in neurons. Science 269: 549-552.
34. Lutfalla G, Holland SJ, Cinato E, Monneron D, Reboul J, et al. (1995) Mutant U5A cells are complemented by an interferon-α/β receptor subunit generated by alternative processing of a new member of a cytokine receptor gene cluster. EMBO J 14: 5100-5108.
35. Cohen B, Novick D, Barak S, Rubinstein M, (1995) Ligand-induced association of the type I interferon receptor components. Mol Cell Biol 15: 4208-4214.
36. Gazziola C, Cordani N, Carta S, De Lorenzo E, Colombatti A, et al. (2005) The relative endogenous expression levels of the IFNAR2 isoforms influence the cytostatic and pro-apoptotic effect of IFNα on pleomorphic sarcoma cells. Int J Oncol 26: 129-140.
37. Hardy MP, Owczarek CM, Trajanovska S, Liu X, Kola I, et al. (2001) The soluble murine type I interferon receptor Ifnar-2 is present in serum, is independently regulated, and has both agonistic and antagonistic properties. Blood 97: 473-482.
38. Haller O, Stertz S, Kochs G, (2007) The Mx GTPase family of interferon-induced antiviral proteins. Microbes Infect 9: 1636-1643.
39. Honda K, Taniguchi T, (2006) IRFs: master regulators of signalling by Toll-like receptors and cytosolic pattern-recognition receptors. Nat Rev Immunol 6: 644-658.
40. Bianchi TI, Aviles G, Sabattini MS, (1997) Biological characteristics of an enzootic subtype of western equine encephalomyelitis virus from Argentina. Acta Virol 41: 13-20.
41. Schoepp RJ, Smith JF, Parker MD, (2002) Recombinant chimeric western and eastern equine encephalitis viruses as potential vaccine candidates. Virology 302: 299-309.
42. Reed DS, Larsen T, Sullivan LJ, Lind CM, Lackemeyer MG, et al. (2005) Aerosol exposure to western equine encephalitis virus causes fever and encephalitis in cynomolgus macaques. J Infect Dis 192: 1173-1182.
43. Cohen MA, Itsykson P, Reubinoff BE (2007) Neural differentiation of human ES cells. Curr Protoc Cell Biol Chapter 23: Unit 23 27.
44. Pankratz MT, Li XJ, Lavaute TM, Lyons EA, Chen X, et al. (2007) Directed neural differentiation of human embryonic stem cells via an obligated primitive anterior stage. Stem Cells 25: 1511-1520.
45. Ma W, Tavakoli T, Derby E, Serebryakova Y, Rao MS, et al. (2008) Cell-extracellular matrix interactions regulate neural differentiation of human embryonic stem cells. BMC Dev Biol 8: 90.
46. Wang TW, Stromberg GP, Whitney JT, Brower NW, Klymkowsky MW, et al. (2006) Sox3 expression identifies neural progenitors in persistent neonatal and adult mouse forebrain germinative zones. J Comp Neurol 497: 88-100.
47. Lendahl U, Zimmerman LB, McKay RD, (1990) CNS stem cells express a new class of intermediate filament protein. Cell 60: 585-595.
48. Sarnat HB, Nochlin D, Born DE, (1998) Neuronal nuclear antigen (NeuN): a marker of neuronal maturation in early human fetal nervous system. Brain Dev 20: 88-94.
49. Shaw G, Weber K, (1982) Differential expression of neurofilament triplet proteins in brain development. Nature 298: 277-279.
50. Gaspard N, Vanderhaeghen P, (2011) From stem cells to neural networks: recent advances and perspectives for neurodevelopmental disorders. Dev Med Child Neurol 53: 13-17.
51. Wen Y, Chen B, Ildstad ST, (2011) Stem cell-based strategies for the treatment of type 1 diabetes mellitus. Expert Opin Biol Ther 11: 41-53.
52. Kattman SJ, Koonce CH, Swanson BJ, Anson BD, (2011) Stem cells and their derivatives: a renaissance in cardiovascular translational research. J Cardiovasc Transl Res 4: 66-72.
53. Jakel RJ, Schneider BL, Svendsen CN, (2004) Using human neural stem cells to model neurological disease. Nat Rev Genet 5: 136-144.
54. Markus A, Grigoryan S, Sloutskin A, Yee MB, Zhu H, et al. (2011) Varicella-zoster virus (VZV) infection of neurons derived from human embryonic stem cells: direct demonstration of axonal infection, transport of VZV, and productive neuronal infection. J Virol 85: 6220-6233.
55. Dukhovny A, Sloutskin A, Markus A, Yee MB, Kinchington PR, et al. (2012) Varicella-zoster virus infects human embryonic stem cell-derived neurons and neurospheres but not pluripotent embryonic stem cells or early progenitors. J Virol 86: 3211-3218.
56. Cho MS, Lee YE, Kim JY, Chung S, Cho YH, et al. (2008) Highly efficient and large-scale generation of functional dopamine neurons from human embryonic stem cells. Proc Natl Acad Sci U S A 105: 3392-3397.
57. Sabin AB, (1947) Epidemic encephalitis in military personnel; isolation of Japanese B virus on Okinawa in 1945, serologic diagnosis, clinical manifestations, epidemiologic aspects and use of mouse brain vaccine. J Am Med Assoc 133: 281-293.
58. Dickerson RB, Newton JR, Hansen JE, (1952) Diagnosis and immediate prognosis of Japanese B encephalitis; observations based on more than 200 patients with detailed analysis of 65 serologically confirmed cases. Am J Med 12: 277-288.
59. Moisse K, Strong MJ, (2006) Innate immunity in amyotrophic lateral sclerosis. Biochim Biophys Acta 1762: 1083-1093.
60. Eantuzzi L, Eid P, Malorni W, Rainaldi G, Gauzzi MC, et al. (1997) Post-translational up-regulation of the cell surface-associated alpha component of the human type I interferon receptor during differentiation of peripheral blood monocytes: role in the biological response to type I interferon. Eur J Immunol 27: 1075-1081.
61. Zurney J, Howard KE, Sherry B, (2007) Basal expression levels of IFNAR and Jak-STAT components are determinants of cell-type-specific differences in cardiac antiviral responses. J Virol 81: 13668-13680.
62. van Boxel-Dezaire AH, Rani MR, Stark GR, (2006) Complex modulation of cell type-specific signaling in response to type I interferons. Immunity 25: 361-372.
63. Du Z, Wei L, Murti A, Pfeffer SR, Fan M, et al. (2007) Non-conventional signal transduction by type 1 interferons: the NF-κB pathway. J Cell Biochem 102: 1087-1094.
64. Pestka S, (2007) The interferons: 50 years after their discovery, there is much more to learn. J Biol Chem 282: 20047-20051.
65. de Weerd NA, Samarajiwa SA, Hertzog PJ, (2007) Type I interferon receptors: biochemistry and biological functions. J Biol Chem 282: 20053-20057.
66. Wellen J, Walter J, Jangouk P, Hartung HP, Dihne M, (2009) Neural precursor cells as a novel target for interferon-β. Neuropharmacology 56: 386-398.
67. Akwa Y, Hassett DE, Eloranta ML, Sandberg K, Masliah E, et al. (1998) Transgenic expression of IFN-α in the central nervous system of mice protects against lethal neurotropic viral infection but induces inflammation and neurodegeneration. J Immunol 161: 5016-5026.
68. Reinarz AB, Broome MG, Sagik BP, (1971) Age-dependent resistance of mice to Sindbis virus infection: viral replication as a function of host age. Infect Immun 3: 268-273.
69. Pattyn SR, De Vleesschauwer L, Van der GG, (1975) Replication of arboviruses in mouse organ cultures. II. Multiplication of virulent and avirulent Semliki Forest and western equine encephalitis viruses in mouse organ cultures. Arch Virol 49: 33-37.
70. Griffin DE, (1976) Role of the immune response in age-dependent resistance of mice to encephalitis due to Sindbis virus. J Infect Dis 133: 456-464.
71. Fazakerley JK, Pathak S, Scallan M, Amor S, Dyson H, (1993) Replication of the A7(74) strain of Semliki Forest virus is restricted in neurons. Virology 195: 627-637.
72. Steele KE, Twenhafel NA, (2010) REVIEW PAPER: pathology of animal models of alphavirus encephalitis. Vet Pathol 47: 790-805.
73. Porret A, Merillat AM, Guichard S, Beermann F, Hummler E, (2006) Tissue-specific transgenic and knockout mice. Methods Mol Biol 337: 185-205.